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Sleeping on the wing
Abstract
Wakefulness enables animals to interface adaptively with the environment. Paradoxically, in insects to humans, the efficacy of wakefulness depends on daily sleep, a mysterious, usually quiescent state of reduced environmental awareness. However, several birds fly non-stop for days, weeks or months without landing, questioning whether and how they sleep. It is commonly assumed that such birds sleep with one cerebral hemisphere at a time (i.e. unihemispherically) and with only the corresponding eye closed, as observed in swimming dolphins. However, the discovery that birds on land can perform adaptively despite sleeping very little raised the possibility that birds forgo sleep during long flights. In the first study to measure the brain state of birds during long flights, great frigatebirds (Fregata minor) slept, but only during soaring and gliding flight. Although sleep was more unihemispheric in flight than on land, sleep also occurred with both brain hemispheres, indicating that having at least one hemisphere awake is not required to maintain the aerodynamic control of flight. Nonetheless, soaring frigatebirds appeared to use unihemispheric sleep to watch where they were going while circling in rising air currents. Despite being able to engage in all types of sleep in flight, the birds only slept for 0.7 h d⁻¹ during flights lasting up to 10 days. By contrast, once back on land they slept 12.8 h d⁻¹. This suggests that the ecological demands for attention usually exceeded that afforded by sleeping unihemispherically. The ability to interface adaptively with the environment despite sleeping very little challenges commonly held views regarding sleep, and therefore serves as a powerful system for examining the functions of sleep and the consequences of its loss. © 2016 The Author(s) Published by the Royal Society. All rights reserved.
... Historically, it was assumed that birds sleep unihemispherically during long flights [81]. This stemmed from the discovery that mallards (Anas platyrhynchos) sleeping on land can switch from sleeping with both eyes closed and both hemispheres (bihemispherically) when safe to sleeping with one eye open (unihemispherically) when threatened [2]. ...
... Photo by Vivek Khanzodé, reproduced from [92]. Illustration by Damond Kyllo, reproduced from [81]. ...
The evolutionary origins of sleep and its sub-states, rapid eye movement (REM) and non-REM (NREM) sleep, found in mammals and birds, remain a mystery. Although the discovery of a single type of sleep in jellyfish suggests that sleep evolved much earlier than previously thought, it is unclear when and why sleep diversified into multiple types of sleep. Intriguingly, multiple types of sleep have recently been found in animals ranging from non-avian reptiles to arthropods to cephalopods. Although there are similarities between these states and those found in mammals and birds, notable differences also exist. The diversity in the way sleep is expressed confounds attempts to trace the evolution of sleep states, but also serves as a rich resource for exploring the functions of sleep.
... When did they sleep? Due to the size mismatch between tiny avian subjects and large experimental recording apparatus, studies have been limited (Rattenborg et al., 2000;Rattenborg, 2017). Scientists hypothesized, based on visual observations and indirect studies, that birds might fly either using only one hemisphere (UHS), or simply lock their wings and glide (BHS), supported by the evidence that birds are still capable of flight after the connections between the brain and the spinal cord had been severed (Rattenborg et al., 2000). ...
... Indeed, due to newer tracking capabilities, it has been found that great frigatebirds (Fregata minor) do utilize both UHS and BHS while they fly. However, the amount of time they spend sleeping during flight was surprisingly small, less than an hour per day (mostly UHS or asymmetric sleep), in contrast to nearly 13 h of sleep per day while nesting (Rattenborg, 2017). ...
We model the dynamics of sleep states in two connected model brain hemispheres, using groups of coupled individual Hindmarsh-Rose neural oscillators. In a single isloated hemisphere, sleep-promoting neurons and wake-promoting neurons exhibit alternating levels of within-group mean field activity, as well as alternating levels of stochastic phase synchronization, as the system moves between simulated day and night. In a two-hemisphere model, we find differences in the behavior of the sleep-promototing or wake-promoting regions between hemispheres, indicative of chimera-like behavior. We observe phase-cluster states, in which different hemispheres exhibit different bursting dynamics, as well as differences in synchronization between hemispheres. This provides a basis for modeling unihemispheric sleep, which occurs naturally in cetaceans and some bird species, among others, as well as asymmetric sleep, which occurs in human subjects suffering from sleep apnea or experiencing the “first night effect” induced by sleeping in a novel environment.
... It has been previously suggested that, at least in some brain regions, neuronal activity during stereotypic running is functionally closer to sleep than to an awake state dominated by goal-directed purposeful behaviour [5]. This notion is consistent with the finding that several animal species can reduce their sleep time dramatically when prolonged wakefulness is ecologically relevant or not optional, such as in some species of birds during migration [41,42] or in marine mammals [43][44][45]. It is likely, therefore, that substantial differences in the amount of sleep between species and at the individual level may be related to qualitative differences in waking behaviour, in addition to the need to satisfy fundamental biological drives such as reproduction [37]. ...
... For example, when sleep-like activity occurs during wakefulness in brain areas not directly involved in task execution, essential behavioural performance could be maintained for extensive periods of time. This has previously been shown in great frigate birds who stay in the air for many days while, intermittently, entering mostly unihemispheric sleep, correlated with gliding flight but not manoeuvring [41,42]. Here, we propose that the notion of maintaining certain wake behaviours during mixed states might not be specific to certain species but could be a wider phenomenon. ...
Background
Homeostatic regulation of sleep is reflected in the maintenance of a daily balance between sleep and wakefulness. Although numerous internal and external factors can influence sleep, it is unclear whether and to what extent the process that keeps track of time spent awake is determined by the content of the waking experience. We hypothesised that alterations in environmental conditions may elicit different types of wakefulness, which will in turn influence both the capacity to sustain continuous wakefulness as well as the rates of accumulating sleep pressure. To address this, we compared the effects of repetitive behaviours such as voluntary wheel running or performing a simple touchscreen task, with wakefulness dominated by novel object exploration, on sleep timing and EEG slow-wave activity (SWA) during subsequent NREM sleep.
Results
We find that voluntary wheel running is associated with higher wake EEG theta-frequency activity and results in longer wake episodes, as compared with exploratory behaviour; yet, it does not lead to higher levels of EEG SWA during subsequent NREM sleep in either the frontal or occipital derivation. Furthermore, engagement in a touchscreen task, motivated by food reward, results in lower SWA during subsequent NREM sleep in both derivations, as compared to exploratory wakefulness, even though the total duration of wakefulness is similar.
Conclusion
Overall, our study suggests that sleep-wake behaviour is highly flexible within an individual and that the homeostatic processes that keep track of time spent awake are sensitive to the nature of the waking experience. We therefore conclude that sleep dynamics are determined, to a large degree, by the interaction between the organism and the environment.
... It has been previously suggested that, at least in some brain regions, neuronal activity during stereotypic running is functionally closer to sleep than to an awake state dominated by goal-directed purposeful behaviour (Fisher et al., 2016). This notion is consistent with the finding that several animal species can reduce their sleep time dramatically when prolonged wakefulness is ecologically relevant or no longer optional, such as in some species of birds during migration (Rattenborg et al., 2016;Rattenborg, 2017) or in marine mammals (Mukhametov, 1987;Lyamin, 1993;Lyamin et al., 2008). It is likely, therefore, that substantial differences in the amount of sleep between species and at the individual level may be related to qualitative differences in waking behaviour, in addition to the need to satisfy fundamental biological drives such as reproduction (Lesku et al., 2012). ...
... For example, when sleep-like activities occur during wakefulness in brain areas not directly involved in task execution, essential behavioural performance could be maintained for extensive periods of time. This has previously been shown in great frigate birds who stay in the air for up to ten days while, intermittently, entering mostly unihemispheric sleep, correlated with stereotypical gliding flight but not manoeuvring (Rattenborg et al., 2016;Rattenborg, 2017). Here we propose that the notion of maintaining certain wake behaviours during mixed states might not be specific to certain species but could be a wider phenomenon. ...
Homeostatic regulation of sleep is reflected in the maintenance of a daily balance between sleep and wake. Although numerous internal and external factors can influence sleep, it is unclear whether and to what extent the process that keeps track of time spent awake is determined by the content of the waking experience. We hypothesised that alterations in environmental conditions may elicit different types of wakefulness, which will in turn influence both the capacity to sustain continuous wakefulness as well the rates of accumulating sleep pressure. To address this, we performed two experiments, where we compared wakefulness dominated by novel object exploration with either (i) the effects of voluntary wheel running (Experiment 1) or (ii) performance in a simple touchscreen task (Experiment 2). We find that voluntary wheel running results in longer wake episodes, as compared with exploratory behaviour; yet it does not lead to higher levels of EEG slow wave activity (SWA) during subsequent sleep. On the other hand, engagement in a touchscreen task, motivated by a food reward, results in lower SWA during subsequent sleep, as compared to exploratory wakefulness, even though the total duration of wakefulness was similar. Overall, our study suggests that sleep-wake behaviour is highly flexible within an individual, and that the homeostatic process that keeps track of time spent awake is sensitive to the nature of the waking experience. We therefore conclude that sleep dynamics are determined, to a large degree, by the interaction between the organism and the environment.
... Several avian species engage in long, non-stop flights: bar-tailed godwits (Limosa lapponica baueri) fly from Alaska to New Zealand in 8.1 days spanning 11,690 km of sustained flight (Gill et al., 2009); great frigatebirds fly around the Indian Ocean for up to 2 months without landing on the water (Weimerskirch et al., 2016); and Alpine swifts (Tachymarptis melba) and Common swifts (Apus apus) can fly for 200 and 300 days, respectively (Liechti et al., 2013;Hedenström et al., 2016). Many other birds also make multiday, non-stop flights (reviewed in Rattenborg, 2017). The discovery that dolphins can swim in a coordinated manner during unihemispheric sleep and ducks can switch to asymmetric sleep when needed on the ground, led to the assumption that flying birds maintain aerodynamic control and navigation by sleeping with one eye open (Rattenborg, 2017). ...
... Many other birds also make multiday, non-stop flights (reviewed in Rattenborg, 2017). The discovery that dolphins can swim in a coordinated manner during unihemispheric sleep and ducks can switch to asymmetric sleep when needed on the ground, led to the assumption that flying birds maintain aerodynamic control and navigation by sleeping with one eye open (Rattenborg, 2017). ...
Birds exhibit two types of sleep that are in many respects similar to mammalian rapid eye movement (REM) and non-REM (NREM) sleep. As in mammals, several aspects of avian sleep can occur in a local manner within the brain. Electrophysiological evidence of NREM sleep occurring more deeply in one hemisphere, or only in one hemisphere - the latter being a phenomenon most pronounced in dolphins - was actually first described in birds. Such asymmetric or unihemispheric NREM sleep occurs with one eye open, enabling birds to visually monitor their environment for predators. Frigatebirds primarily engage in this form of sleep in flight, perhaps to avoid collisions with other birds. In addition to interhemispheric differences in NREM sleep intensity, the intensity of NREM sleep is homeostatically regulated in a local, use-depended manner within each hemisphere. Furthermore, the intensity and temporo-spatial distribution of NREM sleep-related slow waves varies across layers of the avian hyperpallium - a primary visual area - with the slow waves occurring first in, and propagating through and outward from, thalamic input layers. Slow waves also have the greatest amplitude in these layers. Although most research has focused on NREM sleep, there are also local aspects to avian REM sleep. REM sleep-related reductions in skeletal muscle tone appear largely restricted to muscles involved in maintaining head posture. Other local aspects of sleep manifest as a mixture of features of NREM and REM sleep occurring simultaneously in different parts of the neuroaxis. Like monotreme mammals, ostriches often exhibit brainstem-mediated features of REM sleep (muscle atonia and REMs) while the hyperpallium shows EEG slow waves typical of NREM sleep. Finally, although mice show slow waves in thalamic input layers of primary sensory cortices during REM sleep, this is not the case in the hyperpallium of pigeons, suggesting that this phenomenon is not a universal feature of REM sleep. Collectively, the local aspects of sleep described in birds and mammals reveal that wakefulness, NREM sleep, and REM sleep are not always discrete states.
... Finally, a mostly overlooked specialization in animal flight is that birds can sleep on the wing. Rattenborg [5] offers a critical introduction in this poorly understood aerial behaviour and shows how great frigatebirds sleep in unexpected ways and for remarkably small amounts of time. This ability offers new inspiration for managing situational awareness and information processing in flying robots. ...
... (c) Example of how engineers can benefit from new biological discoveries. The poorly understood capacity of some birds, such as the great frigatebird, to sleep on the wing (image credit, Damond Kyllo; [5]) might inspire future aerial robots to budget their situational awareness and signal processing more effectively during extremely long missions. aerodynamics to generate lift. ...
Our understanding of animal flight has inspired the design of new aerial robots with more effective flight capacities through the process of biomimetics and bioinspiration. The aerodynamic origin of the elevated performance of flying animals remains, however, poorly understood. In this themed issue, animal flight research and aerial robot development coalesce to offer a broader perspective on the current advances and future directions in these coevolving fields of research. Together, four reviews summarize and 14 reports contribute to our understanding of low Reynolds number flight. This area of applied aerodynamics research is challenging to dissect due to the complicated flow phenomena that include laminar– turbulent flow transition, laminar separation bubbles, delayed stall and nonlinear vortex dynamics. Our mechanistic understanding of low Reynolds number flight has perhaps been advanced most by the development of dynamically scaled robot models and new specialized wind tunnel facilities: in particular, the tiltable Lund flight tunnel for animal migration research and the recently developed AFAR hypobaric wind tunnel for high-altitude animal flight studies. These world-class facilities are now complemented with a specialized low Reynolds number wind tunnel for studying the effect of turbulence on animal and robot flight in much greater detail than previously possible. This is particular timely, because the study of flight in extremely laminar versus turbulent flow opens a new frontier in our understanding of animal flight. Advancing this new area will offer inspiration for developing more efficient high-altitude aerial robots and removes roadblocks for aerial robots operating in turbulent urban environments. ©2016 The Author(s) Published by the Royal Society. All rights reserved.
... Some birds are capable of remarkable feats of flying that impinge upon achieving a daily amount of sleep 44 . Notably, the great frigatebird (Fregata minor) is a large seabird that soars over the ocean in pursuit of sub-surface prey. ...
Sleep serves many important functions. And yet, emerging studies over the last decade indicate that some species routinely sleep little, or can temporarily restrict their sleep to low levels, seemingly without costs. Taken together, these systems challenge the prevalent view of sleep as an essential state on which waking performance depends. Here, we review diverse case-studies, including elephant matriarchs, post-partum cetaceans, seawater sleeping fur seals, soaring seabirds, birds breeding in the high Arctic, captive cavefish, and sexually-aroused fruit flies. We evaluate the likelihood of mechanisms that might allow more sleep than is presently appreciated. But even then, it appears these species are indeed performing well on little sleep. The costs, if any, remain unclear. Either these species have evolved a (yet undescribed) ability to supplant sleep need, or they endure a (yet undescribed) cost. In both cases, there is urgent need for the study of non-traditional species so we can fully appreciate the extent, causes, and consequences of ecological sleep loss.
... In a review of sleep in flying animals, Rattenborg (2017) concluded, "[I]f for some reason sleep is not possible during flapping flight, then species that primarily rely on this flight mode (e.g., brant, shorebirds, and songbirds) might not sleep on the wing. " A lack of proper sleep is indeed suggested by the observations made on shorebirds after their arrival in New Zealand. ...
... In a review of sleep in flying animals, Rattenborg (2017) concluded, "[I]f for some reason sleep is not possible during flapping flight, then species that primarily rely on this flight mode (e.g., brant, shorebirds, and songbirds) might not sleep on the wing. " A lack of proper sleep is indeed suggested by the observations made on shorebirds after their arrival in New Zealand. ...
The Pacific Basin, by virtue of its vastness and its complex aeroscape, provides unique opportunities to address questions about the behavioral and physiological capabilities and mechanisms through which birds can complete spectacular flights. No longer is the Pacific seen just as a formidable barrier between terrestrial habitats in the north and the south, but rather as a gateway for specialized species, such as shorebirds, to make a living on hemispherically distributed seasonal resources. This recent change in perspective is dramatic, and the research that underpins it has presented new opportunities to learn about phenomena that often challenge a sense of normal. Ancient Polynesians were aware of the seasonal passage of shorebirds and other landbirds over the Pacific Ocean, incorporating these observations into their navigational “tool kit” as they explored and colonized the Pacific. Some ten centuries later, systematic visual observations and tracking technology have revealed much about movement of these shorebirds, especially the enormity of their individual nonstop flights. This invites a broad suite of questions, often requiring comparative studies with bird migration across other ocean basins, or across continents. For example, how do birds manage many days of nonstop exercise apparently without sleep? What mechanisms explain birds acting as if they possess a Global Positioning System? How do such extreme migrations evolve? Through advances in both theory and tracking technology, biologists are poised to greatly expand the horizons of movement ecology as we know it. In this integrative review, we present a series of intriguing questions about trans-Pacific migrant shorebirds and summarize recent advances in knowledge about migratory behavior operating at temporal scales ranging from immediate decisions during a single flight, to adaptive learning throughout a lifetime, to evolutionary development of migratory pathways. Recent advances in this realm should stimulate future research across the globe and across a broad array of disciplines.
... Neural mechanisms controlling social cognition and sexual interactions in birds cannot be fully understood without knowledge of asymmetries in hemispheric functions. Because avian brain has an asymmetrical structure and lacks major interhemispheric commissure, lateralization of cognitive processing can be seen in every aspect of life of birds (Rogers, 2012), such as sleeping during flight (Rattenborg, 2017), foraging (Alonso, 1998), and social interactions (Vallortigara and Andrew, 1991). This means that looking into lateralized visual behaviors can potentially elucidate both behavioral evolution and its underlying physiological mechanisms. ...
The division of cognitive processing between the two hemispheres of the brain causes lateralized eye use in various behavioral contexts. Generally, visual lateralization is shared among vertebrates to a greater extent, with little interspecific variation. However, previous studies on the visual lateralization in mating birds have shown surprising heterogeneity. Therefore, this systematic review paper summarized and analyzed them using phylogenetic comparative methods. The review aimed to elucidate why some species used their left eye and others their right to fixate on individuals of the opposite sex, such as mating partners or prospective mates. It was found that passerine and non-passerine species showed opposite eye use for mating, which could have stemmed from the difference in altricial vs. precocial development. However, due to the limited availability of species data, it was impossible to determine whether the passerine group or altricial development was the primary factor. Additionally, unclear visual lateralization was found when studies looked at lek mating species and males who performed courtship. These findings are discussed from both evolutionary and behavioral perspectives. Possible directions for future research have been suggested.
... So, exotic birds have led to important findings, such as showing that birds can sleep while flying by studying the brain wave patterns during flying of the large, long-term flier the great frigate bird (Fregata minor) in the Galapagos Islands. Yet, the greater frigate bird is hardly likely to become a true animal model due to the difficulty of access to these birds (Rattenborg, 2017). ...
Biomedical research focusing on physiological, morphological, behavioral, and other aspects of development has long depended upon the chicken (Gallus gallus domesticus) as a key animal model that is presumed to be typical of birds and generally applicable to mammals. Yet, the modern chicken in its many forms is the result of artificial selection more intense than almost any other domesticated animal. A consequence of great variation in genotype and phenotype is that some breeds have inherent aberrant physiological and morphological traits that may show up relatively early in development (e.g., hypertension, hyperglycemia, and limb defects in the broiler chickens). While such traits can be useful as models of specific diseases, this high degree of specialization can color general experimental results and affect their translational value. Against this background, in this review we first consider the characteristics that make an animal model attractive for developmental research (e.g., accessibility, ease of rearing, size, fecundity, development rates, genetic variation, etc.). We then explore opportunities presented by the embryo to adult continuum of alternative bird models, including quail, ratites, songbirds, birds of prey, and corvids. We conclude by indicating that expanding developmental studies beyond the chicken model to include additional avian groups will both validate the chicken model as well as potentially identify even more suitable avian models for answering questions applicable to both basic biology and the human condition.
... However, using such sleep by BHGs would likely enable full restoration of their organisms, as in e.g. great frigatebirds Fregata minor (Rattenborg et al. 2019); but see Rattenborg (2017) speculating that avian species may not Fig. 4 Characteristics of nocturnal and diurnal flights of GPS-tracked black-headed gulls breeding in the colony at Bydgoszcz (BYD-PR) during incubation period: A maximum range of flights (km), B total distance covered (km), C total trip duration (min). Boxplots show the median (band inside the box), the first (25%) and third (75%) quartile (box), the lowest and the highest values within 1.5 interquartile range (whiskers) and outliers (dots) require restoration after sleep deprivation at the expected extent and compared to mammals. ...
Many vertebrates exhibit a diel activity, steered by light–dark cycle. However, some colonial waterbirds, in that several species of gulls, are active not only in day hours but also at night. In this study, we aimed to investigate 24 h cycle of black-headed gulls (BHG) Chroicocephalus ridibundus activity with focus on sleep behaviour. We expected that 24 h patterns of activity differ between colonies located in various habitats, and within a colony between nests located in the centre vs at the edge. We studied behaviour based on 9600 of 30 s videos from camera-traps taken in six colonies and data from 10 GPS-tracked individuals from one colony recorded during incubation. BHGs stayed active on average during 48.1% of a night, mainly spent on passive and active nest defence, and on nest maintenance. BHGs spent similar time on these activities in day hours. Individuals breeding in the colony centre slept at night longer than those at its edge. BHGs stayed active during on average 76.5% of daytime. In two urban colonies with the highest nest densities and highest level of light pollution birds slept less during the day than in other studied colonies (three rural and one urban) characterized by lower densities and light intensity after sunset near the colony. Knowledge of nocturnal behaviour is crucial to comprehend 24 h activity patterns of an organism, especially to understand flexibility of behaviour crucial for restoration, like sleep.
... Still, unihemispheric sleep is likely insufficient over a weeks-long migration (Rattenborg 2017), and given the known effects of slow-wave sleep deficits-for the immune system (Imeri and Opp 2009), cognitive function (Hairston et al. 2005), and daily energy budgeting (Berger andPhillips 1995, Cirelli andTononi 2008)-the role of sleep during stopovers deserves a closer look. Songbirds are occasionally observed sleeping more deeply during stopovers (Németh 2009, Covino andCooney 2015), notably after long endurance flights and when bodily condition is poor (Ferretti et al. 2019). ...
Stopovers comprise a significant proportion of the time that many birds spend migrating, and researchers have long relied on these events to define and classify broader migratory strategies. Analyses of stopovers often assume that individuals stop primarily or exclusively in order to replenish energy stores, but other non-fueling behaviors have also been described during stopover events and can influence stopover incidence and duration. Here, we discuss the growing demand for understanding these non-fueling behaviors and for restoring the inherent behavioral complexity to stopover events. We begin by describing how lightweight tracking technologies allow researchers to follow individuals along their entire migratory journeys, capturing stopovers that controvert the traditional stop-refuel-resume paradigm. We then discuss 5 well-identified non-fueling behaviors-recovering, sleeping, waiting, information gathering, and social interactions-and examine how including these behaviors can alter interpretations of individual movement paths. Finally, we outline emerging directions for identifying these behaviors and look to larger implications for population management and site conservation along migratory flyways.
... The males that are awake the most are more attractive to the females and thus sire the most offspring. Also, several types of birds engage in long, non-stop flights during migration and foraging that seemingly leave little time for sleep [16]. Recently, it has been shown that frigatebirds (Fregata minor) sleep during foraging flights where they stay airborne for 6 consecutive days. ...
Sleep is considered to be of crucial importance for performance and health, yet much of what we know about sleep is based on studies in a few mammalian model species under strictly controlled laboratory conditions. Data on sleep in different species under more natural conditions may yield new insights in the regulation and functions of sleep. We therefore performed a study with miniature electroencephalogram (EEG) data loggers in starlings under semi-natural conditions, group housed in a large outdoor enclosure with natural temperature and light. The birds showed a striking 5-h difference in the daily amount of non-rapid-eye-movement (NREM) sleep between winter and summer. This variation in the amount of NREM sleep was best explained by night length. Most sleep occurred during the night, but when summer nights became short, the animals displayed mid-day naps. The decay of NREM sleep spectral power in the slow-wave range (1.1–4.3 Hz) was steeper in the short nights than in the longer nights, which suggests that birds in summer have higher sleep pressure. Additionally, sleep was affected by moon phase, with 2 h of NREM sleep less during full moon. The starlings displayed very little rapid-eye-movement (REM) sleep, adding up to 1.3% of total sleep time. In conclusion, this study demonstrates a pronounced phenotypical flexibility in sleep in starlings under semi-natural conditions and shows that environmental factors have a major impact on the organization of sleep and wakefulness.
... Sleep deprivation, experienced during periods of nocturnal restlessness, did not affect cognitive abilities of captive passerine migrants with food provided ad libitum [23], yet how wild migrants balance sleep and foraging needs en route remains unknown. One possibility is that they sleep on the wing at night [24]. However, in the only study to demonstrate sleep in flight, great frigatebirds (Fregata minor) slept during soaring, but not flapping, flight [21]. ...
Each spring and fall, millions of normally diurnal birds switch to migrating at night. Most of these are small songbirds (passerine) migrating long distances that need to alternate their migratory flights with refueling stopovers [1, 2], which can account for up to 80% of the total migratory period [3]. After a long nocturnal flight, these birds face the contrasting needs to recover sleep and refill depleted energy stores, all while vulnerable to predation [4, 5]. Here, we investigated how garden warblers at a Mediterranean stopover site modulate their sleep behavior in relation to their metabolic state. At night, garden warblers in poor metabolic condition sleep more and exhibit less migratory restlessness than birds in good condition do. In addition, rather than sleeping with their head facing forward, birds in poor condition prefer to sleep with their head turned and tucked in their feathers. We further show that sleep with the head tucked is associated with lower respiratory and metabolic rates and reduced heat loss mediated by hiding the head-the body part with the highest heat dissipation-under the feathers. However, the benefit of conserving energy while sleeping with the head tucked was countered by reduced anti-predator vigilance. Birds presented with a sound simulating the approach of a predator responded more slowly when the head was tucked than when it was untucked. Consequently, our study demonstrates that through changing their sleep position and intensity, migrating songbirds can negotiate a previously unknown trade-off between sleep-mediated energy conservation and anti-predatory vigilance.
... 76 In addition, flying birds can be grouped broadly into categories based on wing tip shape (rounded, pointed, convex or concave) as well as the aspect ratio of the wing (stubby or slender). 44 Bird species used in flight research include, for example, pigeons, 81 hummingbirds, 83 quail, 3 zebra finches, 77 starlings, 9 corvids, 30 cockatiels, 28 lovebirds, 37 parrotlets, 14 chukar partridge, 7 turkeys, 64 seabirds, 62 hawks, 79 and eagles. 10 Regardless of the model chosen, none of the species of birds just listed are purpose-bred for research; consequently high-quality SPF sources are not readily available. ...
A thorough understanding of how animals fly is a central goal of many scientific disciplines. Birds are a commonly used model organism for flight research. The success of this model requires studying healthy and naturally flying birds in a laboratory setting. This use of a nontraditional laboratory animal species presents unique challenges to animal care staff and researchers alike. Here we review regulatory, animal care, and training considerations associated with avian flight research.
... For instance, in Walt Whitman's poem, "Thou who hast slept all night upon the storm", he envisioned frigatebirds sleeping on the wing. Although animal tracking studies have confirmed that frigatebirds [1] and several other species [2] spend weeks to months flying non-stop, sleep in flight was only recently demonstrated for the first time [3]. ...
... Typically, diurnal songbird migrants sleep far less during their nocturnal migrations than during non-migratory periods (Fuchs et al. 2006), yet they seem to suffer few of the negative consequences so obvious in sleep-deprived mammals (Rattenborg et al. 2004). Sleep prior to departure may help to offset a sleep debt (see Fuchs et al. 2006), and if periods of sleep are semi-hemispheric (Fuchs et al. 2009), migrants could process directional and atmospheric information at the same time that they gain some sleep (see Rattenborg 2017). Finally, a period of inactivity prior to departure may simply reflect reduced foraging efficiency or increased risk of predation (see Beauchamp 2017) as light levels decline. ...
Quiescence is a period of inactivity that occurs before the onset of migratory activity in nocturnally migrating birds. This behavior has been observed in captive birds in migratory disposition, but its occurrence in free-ranging migratory birds has been documented only anecdotally, and causal factors and function(s), if any, are unknown. In this study, we documented and characterized quiescence in three migratory songbird species (red-eyed vireo [Vireo olivaceus], Swainson’s thrush [Catharus ustulatus], and wood thrush [Hylocichla mustelina]) by measuring movement and proportion of time spent inactive prior to departure from a stopover site during fall migration. Individuals of each species displayed a period of inactivity prior to departure which varied from less than 30 min to over 90 min with red-eyed vireos engaged in the longest, most pronounced quiescence. We also examined how quiescence was related to intrinsic and extrinsic factors known to influence the departure of migrating birds, and found some evidence for an effect of age and departure time but no effect of a migrant’s energetic condition, departure direction, atmospheric conditions around departure, or day of year on quiescence. Our novel application of an automated radiotelemetry system yielded a large amount of data to characterize quiescence in free-ranging migratory birds, and we provide guidance for future studies to tease apart the various causal factors and function(s) of this migratory behavior.
Significance statement
Quiescence is a poorly understood period of inactivity observed among captive and free-ranging migratory songbirds prior to the onset of nocturnal activity. Our novel use of automated radiotelemetry revealed quiescence among three intercontinental migratory songbirds. It also enabled us to ask how quiescence might be related to intrinsic and extrinsic factors known to influence the departure of migrating birds, and provided an opportunity to explore possible function(s), if any, of this intriguing behavior.
... Although GPS, satellite and geolocator tags are typically used to track large-scale movements of animals across the globe, they can provide insights into sleep [111]. For example, these tags have uncovered long-lasting movements that seemingly leave little time for sleep (reviewed in [112]). Tracking studies have shown that bar-tailed godwits (Limosa lapponica baueri) fly non-stop from Alaska to New Zealand, a flight spanning 11 680 km and lasting 9 days [113], and GPS has shown that great frigate-birds fly non-stop for up to two months [114]. ...
Despite being a prominent aspect of animal life, sleep and its functions remain poorly understood. As with any biological process, the functions of sleep can only be fully understood when examined in the ecological context in which they evolved. Owing to technological constraints, until recently, sleep has primarily been examined in the artificial laboratory environment. However, new tools are enabling researchers to study sleep behaviour and neurophysiology in the wild. Here, we summarize the various methods that have enabled sleep researchers to go wild, their strengths and weaknesses, and the discoveries resulting from these first steps outside the laboratory. The initial studies to ‘go wild’ have revealed a wealth of interindividual variation in sleep, and shown that sleep duration is not even fixed within an individual, but instead varies in response to an assortment of ecological demands. Determining the costs and benefits of this inter- and intraindividual variation in sleep may reveal clues to the functions of sleep. Perhaps the greatest surprise from these initial studies is that the reduction in neurobehavioural performance resulting from sleep loss demonstrated in the laboratory is not an obligatory outcome of reduced sleep in the wild.
This article is part of the themed issue ‘Wild clocks: integrating chronobiology and ecology to understand timekeeping in free-living animals’.
Elucidating the ecological factors underpinning migratory strategies of seabirds is necessary for understanding resilience to environmental change. Arctic terns Sterna paradisaea breed in the Northern Hemisphere and are unique for the global scale of their migration. Geolocator data from 37 Arctic terns breeding in a low-latitude colony, 10 of which were re-tagged in successive years, were analysed to characterise their migratory behaviour and to test the hypothesis that individuals have repeatable migration strategies. Seawater immersion data suggested a fly-forage strategy, with birds remaining on the wing at night and only foraging during daylight. Southward movement was focused initially along Atlantic eastern-boundary upwelling systems. Most terns then reoriented eastwards, crossing the southern Indian Ocean before moving south to the Antarctic. Foraging intensity differed between migration phases. Indian Ocean foraging locations were diverse, and less frequent over deep ocean basins. Foraging intensity was highest in the later stages of return migration, particularly in and around the Azores Confluence Zone. High movement speeds and foraging intensity on return migration may be adaptations to optimise reproductive success. Some aspects of migration phenology were repeatable between years, but trajectories were displaced by wind. Repeat birds did not use the same foraging areas in different years, and their trajectories across the Indian Ocean also differed. The results of this study suggest that the Indian Ocean crossing is a behaviour pattern, surviving since the last ice age, enabling Arctic terns breeding at low-latitude northwest European colonies to arrive at fragmenting Antarctic sea ice when foraging conditions are suitable.
Common human experience is that a long period without sleep is unsustainable, and it is also detrimental to health and behavior. The powerful and primal urge to sleep after sleep deprivation is intense and seems inescapable. The longer we stay awake, the more we feel the need to sleep, and however much we resist, we will inevitably succumb. Although it is obvious what benefits derive from other common and strong physiological drives, such as hunger, sex, and thirst, it is less obvious what drives us to sleep and what benefits accrue. Understanding the biochemical or circuit basis for the sleep drive could enable the benefits of sleep to be artificially stimulated with a new generation of sedative drugs.
Chronic sleep restriction (CSR) is common in modern society, adversely affecting cognitive performance and health. Yet how it impacts neurons regulating sleep remains unclear. Several studies using mice reported substantial losses of wake-active orexin/hypocretin and locus coeruleus (LC) noradrenergic neurons, but not rapid eye movement sleep-active melanin-concentrating hormone (MCH) neurons, following CSR. Here we used immunohistochemistry and stereology to examine orexin, MCH, and LC noradrenergic neurons in a rat model of CSR that uses programmed wheel rotation (3 hours on/1 hour off; ‘3/1’ protocol). Adult male Wistar rats underwent 1 or 4 cycles of the 4-day 3/1 CSR protocol, with 2-day recovery between cycles in home cages. Time-matched control rats were housed in locked wheels/home cages. We found no significant differences in the numbers of orexin, MCH, and LC noradrenergic neurons following either 1- or 4-cycle CSR protocol compared to respective controls. Similarly, the 4-cycle CSR protocol had no effect on the densities of orexin axon terminals in the LC, noradrenergic dendrites in the LC, and noradrenergic axon terminals in the frontal cortex. Body weights, however, decreased after 1 cycle of CSR, and then increased with diminishing slope over the next 3 cycles. Thus, we found no evidence for loss of orexin or LC noradrenergic neurons following 1 and 4 cycles of the 4-day 3/1 CSR protocol in rats. Differences in CSR protocols and/or possible species differences in neuronal vulnerability to sleep loss may account for the discrepancy between the current results in rats and previous findings in mice.
Most adaptations for migration have a neuroendocrine origin, triggered by changes in photoperiod and the patterns of Earth's magnetic field processed by the brain. Migration phenomenology has been well described in the past decades, yet the genetic structure behind it remains terra incognita. We used RNA-Seq data to investigate which biological functions are linked with the seasonal brain adaptations of a long-distance trans-continental migratory passerine, the Northern Wheatear (Oenanthe oenanthe).
We sequenced the wheatear's transcriptomes at three different stages: lean birds, a characteristic phenotype before the onset of migration, during fattening, and at their maximal migratory body mass. We identified a total of 15,357 genes in the brain of wheatears, of which 84 were differentially expressed. These were mostly related to nervous tissue development, angiogenesis, ATP production, innate immune response, and antioxidant protection, as well as GABA and dopamine signalling. The expression pattern of differentially expressed genes is correlated with typical phenotypic changes before migration, such as hyperphagia, migratory restlessness, and a potential increment in the visual and spatial memory capacities. Our work points out, for future studies, biological functions found to be involved in the development of the migratory phenotype —a unique model to study the core of neural, energetic and muscular adaptations for endurance exercise.
Comparison of wheatears' transcriptomic data with two other studies with similar goals shows no correlation among the trends in the gene expression. It highlights the complexity and diversity of adaptations for long-distance migration in birds.
The goal of the research presented in this chapter is to improve the classification process of electromyography (EMG) signals that are contaminated with noise. If the existence of noise in EMG signals is not accounted for, it can degrade the performance of the classification task. Therefore, it is necessary to utilize an efficient filtering process to improve the classification of EMG signals. Guided by the need to filter the noise out of EMG signals, this chapter proposes to employ a Gaussian smoothing filter (GSF) that is simple in its implementation with an efficient filtering performance. The GSF, which is a Gaussian function, offers equal support in both frequency and time domains, allowing it to yield a performance compromise in removing the noise while preserving high frequency components of EMG signals. It is additionally shown that the use of GSF not only enhances the classification accuracy, but it also reduces the computational time needed in the training and testing of the classification process. To evaluate the performance of the GSF in EMG signals classification problem, two experiments are considered. The first experiment consists of classification of multiple hand gestures using EMG signals and the second experiment considers classifying phases of hand motion for a grasping task. An array of standard classification techniques are considered in both experiments and the use of GSF in filtering out noise is shown to enhance classification accuracy with remarkably reduced computational time for the considered classification techniques. This illustrates the feasibility of GSF in filtering EMG signals for classification tasks. To gain further insights into the GSF, its performance is compared with that of a median filter (MF), one of the well-known filtering techniques. By using the overall classification accuracy as an index of comparison, the GSF is shown to result in a superior classification accuracy, demonstrating its efficacy for EMG signals filtering process. Thus, employing GSF proves to provide enhancement in the classification accuracy and required computational efforts.
Current assessment of resuscitation team performance is often based on evaluations using checklists that evaluate verbal communication. However, highly efficient teams may function with several non-verbal cues that may not be measured by current assessment methods. Previous work assessing these non-verbal cues has been accomplished by tracking head movements in providers which however have not been attempted in trauma teams. We sought to perform a preliminary, proof-of-concept study to assess the ability to perform head tracking during a simulated trauma scenario. We enrolled a convenience sample of two simulated trauma teams utilizing undergraduate health professional students from four disciplines available at our institution: 2nd year Radiologic Science (RS), 4th year Physician Assistant (PA), 2nd year Respiratory Care (RT), and 4th year Registered Nurse (RN) students. Each team performed a simulated trauma resuscitation two times while wearing Xsens® MTw motion trackers to track head movements during the resuscitation. These motions were analyzed using a standard measure of discriminating movement patterns known as the Hurst exponent (H). Pre- and post- communication training movement patterns were compared to establish reliability of H in trainees learning trauma resuscitation. There was no difference between the pre- and post- communication training H values for either roll or yaw for any of the four disciplines indicating that non-verbal communications were avoided. The Hurst exponent reliably measures the direction of focus of the participants during some simulated trauma resuscitation scenarios. Future research will be needed to evaluate this analytic technique across providers and in the clinical setting.
Many microorganisms are alive while suspended in the atmosphere, and some seem to be metabolically active during their time there. One of the most important factors threatening their life and activity is solar ultraviolet (UV) radiation. Quantitative understanding of the spatial and temporal survival patterns in the atmosphere, and of the ultimate deposition of microbes to the surface, is limited by a number factors some of which are discussed here. These include consideration of appropriate spectral sensitivity functions for biological damage (e.g. inactivation), and the estimation of UV radiation impingent on a microorganism suspended in the atmosphere. We show that for several bacteria (E. coli, S. typhimurium, and P. acnes) the inactivation rates correlate well with irradiances weighted by the DNA damage spectrum in the UV-B spectral range, but when these organisms show significant UV-A (or visible) sensitivities, the correlations become clearly non-linear. The existence of these correlations enables the use of a single spectrum (here DNA damage) as a proxy for sensitivity spectra of other biological effects, but with some caution when the correlations are strongly non-linear. The radiative quantity relevant to the UV exposure of a suspended particle is the fluence rate at an altitude above ground, while down-welling irradiance at ground-level is the quantity most commonly measured or estimated in satellite-derived climatologies. Using a radiative transfer model that computes both quantities, we developed a simple parameterization to exploit the much larger irradiance data bases to estimate fluence rates, and present the first fluence-rate based climatology of DNA-damaging UV radiation in the atmosphere.
How predators search for prey is a cornerstone question in behavioural ecology, which has yet to be investigated for animals foraging in 3D airspace. Do insectivorous birds such as swifts (Apodidae), swallows and martins (Hirundinidae) use similar strategies to those performed by terrestrial predators in 2D, or do they rely on different spatial search strategies because of some properties of the aerial open space? We addressed this question in the common swift, one of the most aerial birds, using a novel 3D optical tracking method. The analysis of fine-scale flight tracks revealed how birds distribute their presence in 3D space while foraging near their breeding colony. Common swifts concentrated the time spent per volume unit by adopting a tortuous path, and, to a much lesser extent, by decreasing their movement speed. By independently observing the birds’ posture on tracking images, we were able to identify the occurrence of putative prey captures along flight tracks. We show that swifts’ presence was concentrated mainly in the vicinity of prey captures, unveiling a volume-concentrated search (VCS) strategy in this aerial insectivore. This is an extension in 3D of the area-concentrated search classically described in terrestrial 2D space. VCS can (but does not necessarily) take place in thermal updrafts, where small insects can be concentrated in patches. In contrast to terrestrial and aquatic predators that can easily slow down or stop their movement in profitable places, a different speed–cost relationship underlying aerial movement prevents swifts from stopping in prey patches and explains why these birds rely mainly on movement tortuosity to perform intensive search. Our study thus shows how some physical properties of the environment can modulate the way an animal concentrates its search in profitable places.
Daily, animals need to decide when to stop engaging in cognitive processes and behavioral responses to the environment, and go to sleep. The main processes regulating the daily organization of sleep and wakefulness are circadian rhythms and homeostatic sleep pressure. In addition, motivational processes such as food seeking and predator evasion can modulate sleep/wake behaviors. Here, we discuss the principal processes regulating the propensity to stay awake or go to sleep—focusing on neuronal and behavioral aspects. We first introduce the neuronal populations involved in sleep/wake regulation. Next, we describe the circadian and homeostatic drives for sleep. Then, we highlight studies demonstrating various effects of motivational processes on sleep/wake behaviors, and discuss possible neuronal mechanisms underlying their control.
The common swift (Apus apus) is adapted to an aerial lifestyle, where food and nest material are captured in the air. Observations have prompted scientists to hypothesize that swifts stay airborne for their entire non-breeding period [1, 2], including migration into sub-Saharan Africa [3–5]. It is mainly juvenile common swifts that occasionally roost in trees or buildings before autumn migration when weather is bad [1, 6]. In contrast, the North American chimney swift (Chaetura pelagica) and Vaux's swift (C. vauxi) regularly settle to roost in places like chimneys and buildings during migration and winter [7, 8]. Observations of common swifts during the winter months are scarce, and roost sites have never been found in sub-Saharan Africa. In the breeding season, non-breeding individuals usually spend the night airborne [9], whereas adult nesting birds roost in the nest [1]. We equipped common swifts with a micro data logger with an accelerometer to record flight activity (years 1–2) and with a light-level sensor for geolocation (year 2). Our data show that swifts are airborne for >99% of the time during their 10-month non-breeding period; some individuals never settled, but occasional events of flight inactivity occurred in most individuals. Apparent flight activity was lower during the daytime than during the nighttime, most likely due to prolonged gliding episodes during the daytime when soaring in thermals. Our data also revealed that twilight ascents, previously observed during the summer [10], occur throughout the year. The results have important implications for understanding physiological adaptations to endure prolonged periods of flight, including the need to sleep while airborne.
Dopaminergic ventral tegmental area (VTA) neurons are critically involved in a variety of behaviors that rely on heightened arousal, but whether they directly and causally control the generation and maintenance of wakefulness is unknown. We recorded calcium activity using fiber photometry in freely behaving mice and found arousal-state-dependent alterations in VTA dopaminergic neurons. We used chemogenetic and optogenetic manipulations together with polysomnographic recordings to demonstrate that VTA dopaminergic neurons are necessary for arousal and that their inhibition suppresses wakefulness, even in the face of ethologically relevant salient stimuli. Nevertheless, before inducing sleep, inhibition of VTA dopaminergic neurons promoted goal-directed and sleep-related nesting behavior. Optogenetic stimulation, in contrast, initiated and maintained wakefulness and suppressed sleep and sleep-related nesting behavior. We further found that different projections of VTA dopaminergic neurons differentially modulate arousal. Collectively, our findings uncover a fundamental role for VTA dopaminergic circuitry in the maintenance of the awake state and ethologically relevant sleep-related behaviors.
Many birds fly non-stop for days or longer, but do they sleep in flight and if so, how? It is commonly assumed that flying birds maintain environmental awareness and aerodynamic control by sleeping with only one eye closed and one cerebral hemisphere at a time. However, sleep has never been demonstrated in flying birds. Here, using electroencephalogram recordings of great frigatebirds (Fregata minor) flying over the ocean for up to 10 days, we show that they can sleep with either one hemisphere at a time or both hemispheres simultaneously. Also unexpectedly, frigatebirds sleep for only 0.69 h d À 1 (7.4% of the time spent sleeping on land), indicating that ecological demands for attention usually exceed the attention afforded by sleeping unihemispherically. In addition to establishing that birds can sleep in flight, our results challenge the view that they sustain prolonged flights by obtaining normal amounts of sleep on the wing.
Each year more than two billion songbirds cross the Sahara, but how they perform this formidable task is largely unknown. Using geolocation tracks from 27 pied flycatchers, a nocturnally migrating passerine, we show that most birds made diurnal flights in both autumn and spring. These diurnal flights were estimated to be part of non-stop flights of mostly 40-60 h. In spring, birds flew across the Sahara, while autumn migration probably circumpassed part of the desert, through a long oversea flight. Our data contradict claims that passerines cross the Sahara by intermittent flight and daytime resting. The frequent occurrence of long non-stop flights to cross the desert shows migrants' physiological abilities and poses the question why this would not be the general migration strategy to cross the Sahara.
Over decades it has been unclear how individual migratory songbirds cross large ecological barriers such as seas or deserts. By deploying light-level geolocators on four songbird species weighing only about 12 g, we found that these otherwise mainly nocturnal migrants seem to regularly extend their nocturnal flights into the day when crossing the Sahara Desert and the Mediterranean Sea. The proportion of the proposed diurnally flying birds gradually declined over the day with similar landing patterns in autumn and spring. The prolonged flights were slightly more frequent in spring than in autumn, suggesting tighter migratory schedules when returning to breeding sites. Often we found several patterns for barrier crossing for the same individual in autumn compared to the spring journey. As only a small proportion of the birds flew strictly during the night and even some individuals might have flown non-stop, we suggest that prolonged endurance flights are not an exception even in small migratory species. We emphasise an individual’s ability to perform both diurnal and nocturnal migration when facing the challenge of crossing a large ecological barrier to successfully complete a migratory journey.
Surprisingly little is known about the migration and stopover biology of Ruby-throated Hummingbirds (Archilochus colubris), and even less is known about their sex- or age-dependent migration. First, we provide basic information on the migration and stopover biology of this species along the northern coast of the Gulf of Mexico during autumn, including phenology, stopover duration, fuel deposition rate (FDR), arrival mass, and estimated flight ranges. Second, we investigate whether these stopover variables are influenced by age or sex. Age-dependent migration is expected because young, hatch-year birds on their first migration lack the experience of older individuals. Sex-dependent migration is expected because of sexually dimorphic characteristics in wing morphology and body size. We obtained information on arrival mass, phenology, FDR, stopover duration, and estimated flight ranges through banding data, passive integrated transponder tags, radio telemetry, and color marking at a long-term migration station along the northern coast of the Gulf of Mexico. Our data provide strong evidence for age-dependent migration and only weak evidence for sex-dependent migration. Older birds arrived earlier, had larger fuel loads, and had shorter stopover durations than younger birds. In younger birds, we found no effect of sex on FDR, arrival mass, stopover duration, or phenology. Older males arrived with larger fuel loads than females. Finally, we used flight simulation software and our data to estimate that males and older birds were capable of longer potential flight ranges than either females or younger birds.
You Snooze, You Lose
Sleep serves restorative and memory functions, but it does not always operate analogously across species. Deferral of sleep may be possible when selection strongly favors the awake. Lesku et al. (p. 1654 ; see the Perspective by Siegel ) show that sleep may be deferred without cost or impairment in pectoral sandpipers. These birds breed collectively in the high Arctic, and male competition is intense. Competing for, and displaying to, females are both physically and cognitively demanding, yet birds who slept the least showed no decrease in their ability to perform these activities. Indeed, those males who slept the least obtained the most matings and sired the most offspring.
Significance
Bird migration has captivated the attention of scientists and lay people for centuries, but many unanswered questions remain about how birds negotiate large geographic features during migration. We tracked songbirds across the Gulf of Mexico to investigate the factors associated with birds’ departure decisions, arrival at the Yucatan Peninsula (YP), and crossing times. Our findings suggest that a bird’s fat reserves and low humidity, indicative of favorable synoptic weather patterns, shape departure decisions. Fat, date, and wind conditions predict birds’ detection in the YP. This study highlights the complex decision-making process involved in crossing the Gulf and its effects on migratory routes and speeds. A better understanding of the factors influencing migration across these features will inform conservation of migratory animals.
Understanding and reversing the widespread population declines of birds require estimating the magnitude of all mortality sources. Numerous anthropogenic mortality sources directly kill birds. Cause-specific annual mortality in the United States varies from billions (cat predation) to hundreds of millions (building and automobile collisions), tens of millions (power line collisions), millions (power line electrocutions, communication tower collisions), and hundreds of thousands (wind turbine collisions). However, great uncertainty exists about the independent and cumulative impacts of this mortality on avian populations. To facilitate this understanding, additional research is needed to estimate mortality for individual bird species and affected populations, to sample mortality throughout the annual cycle to inform full life-cycle population models, and to develop models that clarify the degree to which multiple mortality sources are additive or compensatory. We review sources of direct anthropogenic mortality in relation to the fundamental ecological objective of disentangling how mortality sources affect animal populations.
Moving animals connect our world, spreading pollen, seeds, nutrients, and parasites as they go about the their daily lives. Recent integration of high-resolution Global Positioning System and other sensors into miniaturized tracking tags has dramatically improved our ability to describe animal movement. This has created opportunities and challenges that parallel big data transformations in other fields and has rapidly advanced animal ecology and physiology. New analytical approaches, combined with remotely sensed or modeled environmental information, have opened up a host of new questions on the causes of movement and its consequences for individuals, populations, and ecosystems. Simultaneous tracking of multiple animals is leading to new insights on species interactions and, scaled up, may enable distributed monitoring of both animals and our changing environment.
Copyright © 2015, American Association for the Advancement of Science.
Many fundamental aspects of migration remain a mystery, largely due to our inability to follow small animals over vast spatial areas. For more than 50 years, it has been hypothesized that, during autumn migration, blackpoll warblers (Setophaga striata) depart northeastern North America and undertake a non-stop flight over the Atlantic Ocean to either the Greater Antilles or the northeastern coast of South America. Using miniaturized light-level geolocators, we provide the first irrefutable evidence that the blackpoll warbler, a 12 g boreal forest songbird, completes an autumn transoceanic migration ranging from 2270 to 2770 km (mean ± s.d.: 2540 ± 257) and requiring up to 3 days (62 h ± 10) of non-stop flight. This is one of the longest non-stop overwater flights recorded for a songbird and confirms what has long been believed to be one of the most extraordinary migratory feats on the planet.
© 2015 The Author(s) Published by the Royal Society. All rights reserved.
We describe the migration routes and non-breeding areas of Common Terns (Sterna hirundo) from the Azores Archipelago, based on ringing (banding) recoveries and tracking of three birds using geolocators. Over 20 years, there have been 55 transatlantic recoveries of Common Terns from the Azores population: six from Argentina and 49 from Brazil. The three tracked birds migrated south in different months (August, September, November), but the northern migration was more synchronous, with all leaving in April. The birds were tracked to three areas of the South American coast: the male spent November–April on the northern Brazilian coast (13°N–2°S), whereas the two females first spent some time off central-eastern Brazil (4–16°S; one for 1 week, the other for 3 months) and then moved south to the coast of south-eastern Brazil, Uruguay and northern Argentina (24–39°S). Although caution is needed given the small sample size and errors associated with geolocation, the three tracked terns potentially travelled a total of ~23 200 km to and returning from their non-breeding areas, representing an average movement of ~500 km day–1. With the exception of Belém, in northern Brazil, and Lagoa do Peixe, in southern Brazil, the coastal areas used by the tracked birds were also those with concentrations of ringing recoveries, confirming their importance as non-breeding areas for birds from the Azores.
The Papah¯anaumoku¯akea Marine National Monument in the Northwestern Hawaiian Islands protects breeding habitat for many migratory
animals. We used satellite telemetry to describe the areas in which a mobile top predator, the Great Frigatebird Fregata minor, traveled on
foraging trips during the early chick-rearing period from a breeding colony on Tern Island, French Frigate Shoals. Identification of potential
foraging events, indicated by a reduction in transit rate, allowed us to assess whether wide-ranging marine species such as Great Frigatebirds
remain inside the protective boundaries of the Monument while brooding young chicks. Four of 11 foraging trips extended outside of the
boundaries of the Monument. These movements may represent the shortest foraging distances that Great Frigatebirds travel from the colony
because adults need to provision young chicks frequently. We also tracked one male that abandoned its nest on a journey to the southwest
of Tern Island. This bird was tracked for 16 days before the transmitter’s battery expired, and the last transmitted position was nearly 1100
km from Tern Island. These tracks, the first reports of frigatebird telemetry in the Pacific Ocean, provide information about the foraging
behaviors of a top predator during a critical life-history stage—data that will complement tracking data of other species and aid in future
conservation and management decisions concerning the Monument and surrounding waters of the Northwestern Hawaiian Islands.
Radiotelemetry has advanced the field of wildlife biology, especially with the miniaturization of radio-tags. However, the major limitation when radio-tagging birds is the size of the animal to which a radio-tag can be attached. We tested how miniature radio-tags affected flight performance and behavior of Ruby-throated Hummingbirds (Archilochus colubris), possibly the smallest bird species that has been fitted with radio-tags. Using eyelash adhesive, we fitted hatch-year individuals (n ¼ 20 males, n ¼ 15 females) with faux radio-tags of 3 sizes that varied in mass and antenna length (220 mg, 12.7 cm; 240 mg, 12.7 cm; and 220 mg, 6.35 cm), then filmed the birds in a field aviary to quantify activity budgets. We also estimated flight range using flight simulation models. When the 3 radio-tag packages were pooled for analysis, the presence of a radio-tag significantly decreased both flight time (~8%) and modeled flight range (~23%) in comparison to control birds. However, a multiple-comparison analysis between the different packages revealed that there was a significant difference in flight time when the larger radio-tag package (240 mg) was attached, and no significant difference in flight time when the lighter radio-tag packages (220 mg) were attached. Our results are similar to those of other studies that analyzed the flight time or flight range of birds wearing radio-tags. Therefore, currently available lightweight radio-tags (220 mg) may be a new option to aid in the study of hummingbird biology. Future study should focus on the additional drag created by the radio-tag and the effects of the lightest radio-tag packages on free-ranging birds. These studies would provide additional information to determine the feasibility of the use of radio-tags to study hummingbird biology. El impacto de las radio etiquetas en Archilochus colubris
The energy allocation (EA) model defines behavioral strategies that optimize the temporal utilization of energy to maximize reproductive success. This model proposes that all species of the animal kingdom share a universal sleep function that shunts waking energy utilization toward sleep-dependent biological investment. For endotherms, REM sleep evolved to enhance energy appropriation for somatic and CNS-related processes by eliminating thermoregulatory defenses and skeletal muscle tone. Alternating REM with NREM sleep conserves energy by decreasing the need for core body temperature defense. Three EA phenotypes are proposed: sleep-wake cycling, torpor, and continuous (or predominant) wakefulness. Each phenotype carries inherent costs and benefits. Sleep-wake cycling downregulates specific biological processes in waking and upregulates them in sleep, thereby decreasing energy demands imposed by wakefulness, reducing cellular infrastructure requirements, and resulting in overall energy conservation. Torpor achieves the greatest energy savings, but critical biological operations are compromised. Continuous wakefulness maximizes niche exploitation, but endures the greatest energy demands. The EA model advances a new construct for understanding sleep-wake organization in ontogenetic and phylogenetic domains.
Oceans represent extreme ecological barriers for land birds. Yet the Northern Wheatear (Oenanthe oenanthe leucorhoa), a 25-g songbird, negotiates the North Atlantic Ocean twice yearly between Canadian natal and sub-Saharan wintering grounds. Each autumn, these migrants appear to have 2 options: (1) a detour via Greenland, Iceland, and/or Europe to reduce the extent of open-ocean flights or (2) an astonishing nonstop flight of 4,000–5,000 km without resting opportunities between eastern Canada and northwestern Africa. We assessed the feasibility and reliability of nonstop trans-Atlantic migration of Northern Wheatears from Canada to Africa using an individual-based model incorporating flight costs and autumnal wind data from 1979 to 2011. Prevalent wind conditions were supportive of nonstop migration, especially at high altitudes and when winds at departure were favorable. For modeled individuals with high fuel loads, flying at altitudes of ∼3,000 m, successful nonstop trans-Atlantic flights reached Africa on 62% of departure days. On 24% of unsuccessful departure days, individuals could have first stopped in Europe before continuing to Africa. Durations of successful flights varied between 31 and 68 hr, with significantly shorter flights after mid-September. It remains unclear whether natural selection might favor nonstop ocean crossings by O. o. leucorhoa between North America and Africa, but we conclude that reliably supportive winds en route and potentially huge time savings render it a feasible migration strategy.
One of the greatest feats of avian migration is the non-stop crossing of extensive areas of inhospitable habitat such as deserts and seas. Differences in spring and autumn migration routes have been reported in species that cross such barriers, and are thought to have evolved in response to seasonal variation in prevailing wind direction. We tested the hypothesis that migration routes vary seasonally with respect to the Gulf of Mexico in the tree swallow Tachycineta bicolor using solar geolocators attached and retrieved at 4 breeding sites in central North America. We found that 100 % of birds (n = 10) made a trans-Gulf flight of >850 km from Louisiana south to their wintering grounds in the Yucatan Peninsula in 12–36 hours, achieving minimum ground speeds as high as 32 m/s. Although most days during autumn migration were characterized by unfavorable headwinds blowing to the northwest, migration over the Gulf mostly occurred on days with strong winds blowing to the south. In contrast, in 8 of 9 (88 %) of birds on spring migration returned from the wintering grounds towards Louisiana following a clockwise loop pattern flying over land to the west around the Gulf. During this spring period there were few days
with prevailing winds from the south to assist northward migration. Results suggest that, despite being up to three times further (ca. 2,700 km), a coastal circum-Gulf spring migration represents the less risky route when wind conditions are not favorable. These findings also help to resolve a long-standing dispute in the literature concerning migration patterns between the US Gulf coast and Mexico, and provide insight into the factors shaping migration strategies of small songbirds migrating across large bodies of water.
Migrating birds make the longest non‐stop endurance flights in the animal kingdom. Satellite technology is now providing direct evidence on the lengths and durations of these flights and associated staging episodes for individual birds. Using this technology, we compared the migration performance of two subspecies of bar‐tailed godwit Limosa lapponica travelling between non‐breeding grounds in New Zealand (subspecies baueri) and northwest Australia (subspecies menzbieri) and breeding grounds in Alaska and eastern Russia, respectively. Individuals of both subspecies made long, usually non‐stop, flights from non‐breeding grounds to coastal staging grounds in the Yellow Sea region of East Asia (average 10 060 ± SD 290 km for baueri and 5860 ± 240 km for menzbieri). After an average stay of 41.2 ± 4.8 d, baueri flew over the North Pacific Ocean before heading northeast to the Alaskan breeding grounds (6770 ± 800 km). Menzbieri staged for 38.4 ± 2.5 d, and flew over land and sea northeast to high arctic Russia (4170 ± 370 km). The post‐breeding journey for baueri involved several weeks of staging in southwest Alaska followed by non‐stop flights across the Pacific Ocean to New Zealand (11 690 km in a complete track) or stopovers on islands in the southwestern Pacific en route to New Zealand and eastern Australia. By contrast, menzbieri returned to Australia via stopovers in the New Siberian Islands, Russia, and back at the Yellow Sea; birds travelled on average 4510 ± 360 km from Russia to the Yellow Sea, staged there for 40.8 ± 5.6 d, and then flew another 5680–7180 km to Australia (10 820 ± 300 km in total). Overall, the entire migration of the single baueri godwit with a fully completed return track totalled 29 280 km and involved 20 d of major migratory flight over a round‐trip journey of 174 d. The entire migrations of menzbieri averaged 21 940 ± 570 km, including 14 d of major migratory flights out of 154 d total. Godwits of both populations exhibit extreme flight performance, and baueri makes the longest (southbound) and second‐longest (northbound) non‐stop migratory flights documented for any bird. Both subspecies essentially make single stops when moving between non‐breeding and breeding sites in opposite hemispheres. This reinforces the critical importance of the intertidal habitats used by fuelling godwits in Australasia, the Yellow Sea, and Alaska.
In captivity, migratory birds show increased activity during the time that they would normally migrate. The phenology and intensity of such 'migratory restlessness' has been shown to mirror species- and population-specific migration patterns observed in the wild and has consequently been used as a proxy for the motivation to migrate. Many studies doing so, however, were aiming to explain among-individual variation in migratory behaviour or traits, and not species- or population-specific traits. These studies thus assumed that, also at the level of the individual, migratory restlessness is an accurate proxy for the motivation to migrate. We tested this assumption for the first time and found that it holds; individuals showing very little migratory restlessness remained at stopover for longer than one night, whereas most individuals showing more restlessness departed sooner. This finding validates the use of migratory restlessness as a proxy for the motivation to migrate, thereby justifying the conclusions made in a large body of research on avian migration.
Many species travel in highly organized groups. The most quoted function of these configurations is to reduce energy expenditure and enhance locomotor performance of individuals in the assemblage. The distinctive V formation of bird flocks has long intrigued researchers and continues to attract both scientific and popular attention. The well-held belief is that such aggregations give an energetic benefit for those birds that are flying behind and to one side of another bird through using the regions of upwash generated by the wings of the preceding bird, although a definitive account of the aerodynamic implications of these formations has remained elusive. Here we show that individuals of northern bald ibises (Geronticus eremita) flying in a V flock position themselves in aerodynamically optimum positions, in that they agree with theoretical aerodynamic predictions. Furthermore, we demonstrate that birds show wingtip path coherence when flying in V positions, flapping spatially in phase and thus enabling upwash capture to be maximized throughout the entire flap cycle. In contrast, when birds fly immediately behind another bird--in a streamwise position--there is no wingtip path coherence; the wing-beats are in spatial anti-phase. This could potentially reduce the adverse effects of downwash for the following bird. These aerodynamic accomplishments were previously not thought possible for birds because of the complex flight dynamics and sensory feedback that would be required to perform such a feat. We conclude that the intricate mechanisms involved in V formation flight indicate awareness of the spatial wake structures of nearby flock-mates, and remarkable ability either to sense or predict it. We suggest that birds in V formation have phasing strategies to cope with the dynamic wakes produced by flapping wings.
In 2010, following successful trials with geolocators on Ruddy Turnstones in 2009, a total of 105 units, of four different models, were deployed at five locations on Ruddy Turnstones and Greater Sandplovers. Geolocator retrieval rates were 44% on Ruddy Turnstone and 27% on Greater Sandplover. Complete (59%) and partial (15%) technical failure rates on geolocators were high and were mostly the result of wear and saltwater corrosion. All 30 units from the Swiss Ornithological Institute failed. Only half of the Mk10 and Mk12 units from the British Antarctic Survey produced full migration histories. The northward migration of Ruddy Turnstones was on a narrow path with many birds completing an initial non-stop flight of 7,600 km to Taiwan. Later, most made a stopover in the Yellow Sea. Median migration duration was 39.5 days and average migration speed of the first major leg of the journey (assuming the birds followed the great circle route between stopovers) was 63.4 kph. Southward migration paths showed a much wider spread, ranging from Mongolia to the central Pacific. The latter involved the same bird that had been tracked along this route the previous year. It has now been logged on similar 27,000 km round trips in two successive years. The median duration of southward migration (78 days) was nearly twice that of northward migration and data on average migration speed for just two migration legs indicated that it might be lower, 30 and 40 kph being the values recorded. Greater Sandplovers were only tracked on northward migration but seemed to follow a similar migration strategy with a large initial non-stop flight followed by shorter flights and more regular stopovers. Plans are outlined for further analyses and future deployments of geolocators.
Common swifts are specialist flyers spending most of their life aloft, including night-time periods when this species roosts on the wing. Nocturnal roosting is preceded by a vertical ascent in twilight conditions towards altitudes of up to 2.5 km, behaviour previously explained as flight altitude selection for sleeping. We examined the nocturnal flight behaviour of swifts, as uniquely identified by a Doppler weather radar in central Netherlands using continuous measurements during two consecutive breeding seasons. Common swifts performed twilight ascents not only at dusk but also at dawn, which casts new light on the purpose of these ascents. Dusk and dawn ascents were mirror images of each other when time-referenced to the moment of sunset and sunrise, suggesting that the acquisition of twilight-specific light-based cues plays an important role in the progression of the ascents. Ascent height was well explained by the altitude of the 280 K isotherm, and was not significantly related to wind, cloud base height, humidity or the presence of nocturnal insects. We hypothesize that swifts profile the state of the atmospheric boundary layer during twilight ascents and/or attempt to maximize their perceptual range for visual access to distant horizontal landmarks, including surrounding weather. We compare twilight profiling by swifts with vertical twilight movements observed in other taxa, proposed to be related to orientation and navigation.
This study is the first in which light level geolocators (data loggers) were deployed on Pacific Golden-Plovers Pluvialis fulva. In spring 2009 and 2010, we logger-equipped a total of 24 plovers at wintering grounds on Oahu, Hawaii; 22 returned in the subsequent fall migrations, and of these 20 were recaptured. Almost all of the recovered geolocators had archived the full roundtrip to Alaska including nesting locations. Transpacific flights were nonstop along direct north–south pathways. On average, the northward passage required approximately 3 days and covered about 4,800 km; the southward around 4 days and 4,900 km. Ground speeds fluctuated widely during flights (almost certainly because of variable winds); mean ground speeds were estimated at 63 kph in spring, 58 kph in fall. The capacity of this plover for nonstop flight remains unknown; however our results indicate that it exceeds 5 days. All 20 birds nested in southerly parts of the Alaska breeding range, from the Yukon–Kuskokwim Delta to nearly the tip of the Alaska Peninsula, indicating major migratory connectivity between Hawaii and those regions. Geolocator archives during the time birds were on breeding grounds showed periods of successive days with erratic light level patterns (“noise”). Such noise seemed a clear indicator of nesting activities, and also of hatching success or failure.
This is the first comprehensive study of at-sea activity patterns of albatrosses during the nonbreeding period, based on data from combination geolocator-immersion loggers deployed on the wandering albatross Diomedea exulans, black-browed albatross Thalassarche melanophris, greyheaded albatross T. chrysostoma and light-mantled albatross Phoebetria palpebrata from South Georgia (54° 00' S, 38° 03' W). Differences in behaviour among species observed during the breeding season were maintained during the nonbreeding period, suggesting a high degree of foraging niche specialisation. Wandering albatrosses exhibited longer flight bouts, and spent more time on the water during daylight, than any of the smaller species. Light-mantled albatrosses were the most active nocturnally. During daylight, grey-headed albatrosses were the most aerial and black-browed albatrosses had the shortest flight bouts. Although all species still engaged in foraging behaviour predominantly during daylight, they spent a greater proportion of time on the water (presumably resting) during the nonbreeding period compared with the breeding period, suggesting that they could more readily meet their energy demands when no longer subject to central place constraints. There was no evidence from activity patterns that might suggest that wing feather moult handicaps flight capability during the nonbreeding period. Individuals of all species engaged in rapid east-west commutes, when considerably higher proportions of time were spent in flight than while resident, in particular during daylight, possibly because birds are unable to navigate effectively during complete darkness. Despite consistency in individual dispersal patterns, there were year-to-year differences in the nocturnal behaviour of black-browed albatrosses, probably attributable to prey variability.
Although oceanic tropical waters occupy almost 50 % of the total area of pelagic oceans, knowledge of the foraging ecology of top predators in these low productivity waters is limitied. This is particularly the case for tropical seabirds that are believed to rely on scarce and unpredictable resources and have developed specific foraging strategies to exploit these resources. Frigatebirds are tropical seabirds that rely on subsurface predators such as tuna or cetaceans to feed. We studied the foraging strategy at sea of great frigatebirds breeding on Europa Island in the Mozambique Channel using satellite transmitters and altimeters. When foraging, birds moved at slow speeds (average 16.4 km h-1) and stayed at an average altitude of 180 m, continuously climbing and descending. During climbs, they reached high altitudes (maximum 2867 m) and during descent rarely came close to the surface to feed. Birds came to the surface on average 6.2 times d-1. Feeding opportunities occurred only during the day, peaking early in the morning and late in the afternoon. Frigatebirds foraged over extensive distances, up to 612 km from the island, usually during the incubation or post-breeding periods, concentrating their effort in the western oceanic waters of the channel where overall productivity, although low, was still higher than in the eastern part of the channel. The higher productivity in the western waters is due to the presence of a persistent field of mesoscale anticyclonic gyres. Birds tended to avoid the centre of cold eddies and remained at the edge of eddies. When brooding chicks, birds foraged closer to the island, at an average distance of 94 km, mainly in the northwest of the island, in the vicinity of shallow waters of the Bassas da India Bank. During both long and short trips, birds did not return to the same area. Diet was composed essentially of flying-fish and Ommastrephid squids. The results of the study indicate that the strategy of frigatebirds is based on wide ranging foraging directed toward scarce prey patches that are encountered irregularly, and are not predictable in exact location at a coarse scale. At a mesoscale level, birds appear to favour large areas with slightly enhanced productivity such as a zone of strong eddies. Since they feed in close association with subsurface predators, mainly tuna in our area, it can be predicted that large predators such as seabirds or tuna are spread over extensive areas and have an unpredictable localisation at a coarse scale, but have some specific preferences on a regional scale.
Wandering albatrosses were fitted with stomach temperature sensors to detect when they fed. Three birds went to sea for a total of 24 d during which time they ingested 159 prey items which were calculated to have a total mass of 45.65 kg. These results were lumped with results from another study to show that 89% of all prey (by mass) were caught during the day when wandering albatrosses fly the greatest distances. Birds generally rest during periods of darkness but actively search for widely-spaced prey during the day during which time they use dynamic soaring to enable them to cover the requisite large distances with minimal energy expenditure. -Authors
Migratory restlessness-defined as the (mainly nocturnal) migratory activity of caged birds-has been known since at least the 18th Century and is regularly used to study questions regarding bird migration. However, it had not been satisfactorily described until 1988, when we first became able to obtain and analyze video recordings of this behaviour made in infrared light. Thanks to refined video and reproduction techniques, we are now able to present such recordings here, for the first time in printed form (Figs. 1 and 2). The birds involved are first year Blackcaps (Sylvia atricapilla) from southern Germany during their first migration period. According to our experience, the migratory restlessness they show is typical, i.e. not affected by the recording procedure. In the Blackcap-as shown previously for Garden Warblers-by far the most prominent element in this behaviour is typical 'wing whirring': beating the wings while perched, with high frequency and low amplitude. We interpret this 'sedentary migration' as a kind of 'flying with the brakes on' in adaptation to cage conditions. Migratory restlessness, which in addition to whirring includes hopping, climbing, fluttering and flying, is exhibited in all parts of the cage, not only on the perches but also on the floor and walls and even while hanging from the ceiling. Hence theoretically it can be monitored in its entirely only by ultrasound, video technology, bundles of light barriers or cages rigged for general vibration detection. When applied to many experimental animals, however, these methods require elaborate equipment and are susceptible to failure. In our experience the best results are obtained with recording cages having two movable perches mounted on microswitches. If the switch sensitivity is adjusted to the birds' body weight, about 95 % of the migratory restlessness observed in video pictures will be recorded. Because of the large interindividual variation in the parts of the cage where the relevant behaviour occurs and the variability in use of the recording perches, the best measure for quantitative studies of migratory restlessness is not the number of individual events ('hops') but larger-scale units such as half- or whole-hour periods with (or without) migratory activity. In our experience half-hour intervals are quite suitable for many purposes, including quantitative genetic studies.
One of the greatest feats of avian migration is the non-stop crossing of extensive areas of inhospitable habitat such as deserts and seas. Differences in spring and autumn migration routes have been reported in species that cross such barriers, and are thought to have evolved in response to seasonal variation in prevailing wind direction. We tested the hypothesis that migration routes vary seasonally with respect to the Gulf of Mexico in the tree swallow Tachycineta bicolor using solar geolocators attached and retrieved at 4 breeding sites in central North America. We found that 100 % of birds (n = 10) made a trans-Gulf flight of >850 km from Louisiana south to their wintering grounds in the Yucatan Peninsula in 12–36 hours, achieving minimum ground speeds as high as 32 m/s. Although most days during autumn migration were characterized by unfavorable headwinds blowing to the northwest, migration over the Gulf mostly occurred on days with strong winds blowing to the south. In contrast, in 8 of 9 (88 %) birds on spring migration returned from the wintering grounds towards Louisiana following a clockwise loop pat tern flying over land to the west around the Gulf. During this spring period there were few days with prevailing winds from the south to assist northward migration. Results suggest that, despite being up to three times further (ca. 2,700 km), a coastal cir- cum-Gulf spring migration represents the less risky route when wind conditions are not favorable. These findings also help to re solve a long-standing dispute in the literature concerning migration patterns between the US Gulf coast and Mexico, and provide insight into the factors shaping migration strategies of small songbirds migrating across large bodies of water.
Understanding how animals respond to atmospheric conditions across space is critical for understanding the evolution of flight strategies and long-distance migrations. We studied the three-dimensional movements and energetics of great frigate birds (Fregata minor) and showed that they can stay aloft for months during transoceanic flights. To do this, birds track the edge of the doldrums to take advantage of favorable winds and strong convection. Locally, they use a roller-coaster flight, relying on thermals and wind to soar within a 50- to 600-meter altitude band under cumulus clouds and then glide over kilometers at low energy costs. To deal with the local scarcity of clouds and gain longer gliding distances, birds regularly soar inside cumulus clouds to use their strong updraft, and they can reach altitudes of 4000 meters, where freezing conditions occur.
We describe a method and device (< 1.2 g) for recording, processing and storing data about activity and location of individuals of free-living songbirds throughout the annual cycle. Activity level was determined every five minutes from five 100 ms samples of accelerometer data with 5 s between the sampling events. Activity levels were stored on an hourly basis throughout the annual cycle, allowing periods of resting/sleep, continuous flight and intermediate activity (foraging, breeding) to be distinguished. Measurements from a light sensor were stored from preprogrammed key stationary periods during the year to provide control information about geographic location. Successful results, including annual actogram, were obtained for a red-backed shrike Lanius collurio carrying out its annual loop migration between northern Europe and southern Africa. The shrike completed its annual migration by performing > 66 (max. 73) nocturnal migratory flights (29 flights in autumn and > 37, max. 44, in spring) adding up to a total of > 434 (max. 495) flight hours. Migratory flights lasted on average 6.6 h with maximum 15.9 h. These flights were aggregated into eight travel episodes (periods of 4-11 nights when flights took place on the majority of nights). Daytime resting levels were much higher during the winter period compared to breeding and final part of spring migration. Daytime resting showed peaks during days between successive nocturnal flights across Sahara, continental Africa and the Arabian Peninsula, indicating that the bird was mostly sleeping between these long migratory flights. Annual activity and flight data for free-living songbirds will open up many new research possibilities. Main topics that can be addressed are e.g. migratory flight performance (total flight investment, numbers and characteristics of flights), timing of stationary periods, activity patterns (resting/sleep, activity level) in different phases of the annual cycle and variability in the annual activity patterns between and within individuals.
Here, we propose an original approach to explain one of the great unresolved questions in animal biology: what is the function of sleep? Existing ecological and neurological approaches to this question have become roadblocks to an answer. Ecologists typically treat sleep as a simple behavior, instead of a heterogeneous neurophysiological state, while neuroscientists generally fail to appreciate the critical insights offered by the consideration of ecology and evolutionary history. Redressing these shortfalls requires cross-disciplinary integration. By bringing together aspects of behavioral ecology, evolution, and conservation with neurophysiology, we can achieve a more comprehensive understanding of sleep, including its implications for adaptive waking behavior and fitness.
We often experience troubled sleep in a novel environment [1]. This is called the first-night effect (FNE) in human sleep research and has been regarded as a typical sleep disturbance [2-4]. Here, we show that the FNE is a manifestation of one hemisphere being more vigilant than the other as a night watch to monitor unfamiliar surroundings during sleep [5, 6]. Using advanced neuroimaging techniques [7, 8] as well as polysomnography, we found that the temporary sleep disturbance in the first sleep experimental session involves regional interhemispheric asymmetry of sleep depth [9]. The interhemispheric asymmetry of sleep depth associated with the FNE was found in the default-mode network (DMN) involved with spontaneous internal thoughts during wakeful rest [10, 11]. The degree of asymmetry was significantly correlated with the sleep-onset latency, which reflects the degree of difficulty of falling asleep and is a critical measure for the FNE. Furthermore, the hemisphere with reduced sleep depth showed enhanced evoked brain response to deviant external stimuli. Deviant external stimuli detected by the less-sleeping hemisphere caused more arousals and faster behavioral responses than those detected by the other hemisphere. None of these asymmetries were evident during subsequent sleep sessions. These lines of evidence are in accord with the hypothesis that troubled sleep in an unfamiliar environment is an act for survival over an unfamiliar and potentially dangerous environment by keeping one hemisphere partially more vigilant than the other hemisphere as a night watch, which wakes the sleeper up when unfamiliar external signals are detected.
Fall migrations of brent from Izembek Lagoon, Alaska, to wintering areas in Baja California, Mexico were studied from 1959-1988. Surface and upper air weather patterns were analyzed for departure, approximate mid-route and arrival locations. Based on radar observations, upper air wind directions at the 850 millibar level were used to estimate the most favourable migration route to wintering areas in Mexico. Estimated migration routes averaged 5301 km vs a direct route distance of 4408 km. Estimated time in route averaged 54.3 hr and average ground speed was 99 kph based on probable routes. During 1974, 1983 and 1984, observers in Alaska and Mexico documented brent departures and arrivals, estimating times en route to be 60, 60 and 95 hours, respectively. The configuration of the departure weather system, and the direction and velocity of winds, are important factors causing variability in observed flight duration. The rapid fall migration of Pacific populations of brent is energetically costly with males and females, respectively, losing an estimated 33% and 31% of their total body weights. Physiological demands of migration from Izembek Lagoon to Mexico may exceed the amounts of body reserves accumulated during the fall staging period. -from Author
In colour polymorphic species morphs are considered to be adaptations to different environments, where they have evolved and are maintained because of their differential sensitivity to the environment. In cold environments the plumage insulation capacity is essential for survival and it has been proposed that plumage colour is associated with feather structure and thereby the insulation capacity of the plumage. We studied the structure of contour feathers in the colour polymorphic tawny owl (Strix aluco). A previous study of tawny owls in the same population has found strong selection against the brown morph in cold and snowy winters whereas this selection pressure is absent in mild winters. We predicted that grey morphs have a denser and more insulative plumage, enabling them to survive better in cold climate compared to brown ones. The insulative plumulaceous part of the dorsal contour feathers was larger and the fine structure of the plumulaceous part of the feather was denser in grey tawny owls than in brown ones. In the ventral contour feathers the plumulaceous part of the feather was denser in females than in males and in older birds without any differences between morphs. Our study suggests that insulative microscopical feather structures differ between colour morphs and we propose that feather structure may be a trait associated with morph-specific survival in cold environments.This article is protected by copyright. All rights reserved.
Orexins (hypocretins) are two peptides (orexin A and B) produced from the pre-pro-orexin precursor and expressed in a limited region of dorsolateral hypothalamus. Orexins were originally thought to specifically mediate feeding and promote wakefulness, but it is now clear that they participate in a wide range of behavioral and physiological processes under select circumstances. Orexins primarily mediate behavior under situations of high motivational relevance, such as during physiological need states, exposure to threats or reward opportunities. We hypothesize that many behavioral functions of orexins (including regulation of sleep/wake cycling) reflect a fundamentally integrated function for orexins in translating motivational activation into organized suites of psychological and physiological processes supporting adaptive behaviors. We also discuss how numerous forms of neural heterogeneity modulate this function, allowing orexin neurons to organize diverse, adaptive responses in a variety of motivationally relevant situations. Thus, the involvement of orexins in diverse behaviors may reflect a common underlying function for this peptide system.
Significance
A fossil species of pelagornithid bird exhibits the largest known avian wingspan. Pelagornithids are an extinct group of birds known for bony tooth-like beak projections, large size, and highly modified wing bones that raise many questions about their ecology. At 6.4 m, the wingspan of this species was approximately two times that of the living Royal Albatross. Modeling of flight parameters in this species indicates that it was capable of highly efficient gliding and suggests that pelagornithids exploited a long-range marine soaring strategy similar, in some ways, to that of extant albatrosses.
The highly pneumatic skeleton of the extinct flying pterosaurs suggests that they would float high up on open water, but in a posture rather different to that of birds. However, the exact posture of the body and head remains unknown and would be critical for an ocean going pterosaur forced onto the waters' surface or animals that alighted to feed. Using computational methods with recent models and body mass estimates for four pterosaur genera—Dimorphodon, Rhamphorhynchus, Pteranodon and Dsungaripterus we show that the floating posture of pterodactyloid pterosaurs led to the head, neck and body being horizontal with the ventral 1/4 to 1/3 being immersed, and the external nares being almost at, or potentially partially below, the waterline that could have left them vulnerable to drowning. The floatation methods were verified using a model of a Canada goose (Branta canadensis) that is able to successfully replicate the expected orientation and depth of immersion of the bird. While there is convincing ev'idence for a number of pterosaurs foraging in marine and freshwater environments, these results suggest that many did not regularly rest on the surface of the water and if immersed would need to take off again rapidly. The high numbers of fossils of juvenile pterosaurs compared to the terrestrial Mesozoic dinosaurs suggest that this may be linked to their floating posture.
Being airborne is considered to be energetically more costly as compared with being on the ground or in water. Birds migrating or foraging while airborne are thought to spend some time resting on the ground or water to recover from these energetically demanding activities. However, for several decades ornithologists have claimed that some swifts may stay airborne for almost their whole lifetime. Here we present the first unequivocal evidence that an individual bird of the Alpine swift (Tachymarptis melba) can stay airborne for migration, foraging and roosting over a period of more than 6 months. To date, such long-lasting locomotive activities had been reported only for animals living in the sea. Even for an aerodynamically optimized bird, like the Alpine swift, flying requires a considerable amount of energy for continuous locomotive control. Our data imply that all vital physiological processes, including sleep, can be perpetuated during flight.
The foraging success of pelagic seabirds and where and when they catch prey has been largely unknown until now. We use satellite transmitters in conjunction with recorders measuring feeding times and masses ingested to show that wandering albatrosses (Diomedea exulans) on foraging trips from the nest encountered prey on average every 4.4 h and consumed 2.1 kg of food daily. They travelled up to 3600 km from the nesting colony in search of scarce prey, mostly pelagic squid. These were distributed without relation to underwater topography, and were principally caught during daylight hours in discrete patches widely separated along the foraging route. When foraging inshore, the birds fed on more localized aggregations of squid and fish on the shelf breaks. These results demonstrate that the foraging patterns of large seabirds such as wandering albatrosses, which rely on scarce prey, can help to increase our knowledge of the distribution and availability of poorly known but widespread species of squid.
SUMMARY 1. All three species were observed in straight flight, and circling in ther- mals, from Flamenco Island, Panama. Measurements were made by or- nithodolite, an instrument which records a series of timed, three- dimensional position estimates, from which speeds, circle diameters and rates of climb can be calculated. 2. Mean lift coefficients in straight glides ranged from 0*72 to 0-84, except in slope soaring, where a mean of 1-6 was recorded for both the frigatebird and black vulture. 3. Mean circling radii were proportional to wing loading, and varied from 12'Om for the frigatebird to 18-0 m for the pelican. Mean rates of climb ranged from 0-fms" 1 for the black vulture to 0-57 ms"1 for the pelican. All species showed mean circling lift coefficients between 1-33 and 1-45, and angles of bank between 22-9° and 24-7°. 4. It is argued that the frigatebird is adapted to stay airborne continuous- ly, day and night, for extended periods, by exploiting thermals over the sea under trade wind cumulus clouds. The low wing loading is seen as an adaptation to circling in narrow thermals, and the low disc loading as an adaptation giving low minimum power, when flapping cannot be avoided. Take-off appears to be possible only by dropping from an elevated perch, not from the ground or water surface. 5. The low aspect-ratio, tip-slotted wings of the black vulture are certain- ly less efficient for soaring, but appear to be better for upward take-off from the ground. The pelican also has tip-slotted wings. Although its aspect ratio is higher, it is still capable of taking off from a level water surface.